Skip to main content

Advertisement

SpringerLink
Log in

An Overview of the Genetics of Plant Response to Salt Stress: Present Status and the Way Forward

  • Published:
Applied Biochemistry and Biotechnology Aims and scope Submit manuscript

Abstract

Salinity is one of the major threats faced by the modern agriculture today. It causes multidimensional effects on plants. These effects depend upon the plant growth stage, intensity, and duration of the stress. All these lead to stunted growth and reduced yield, ultimately inducing economic loss to the farming community in particular and to the country in general. The soil conditions of agricultural land are deteriorating at an alarming rate. Plants assess the stress conditions, transmit the specific stress signals, and then initiate the response against that stress. A more complete understanding of plant response mechanisms and their practical incorporation in crop improvement is an essential step towards achieving the goal of sustainable agricultural development. Literature survey shows that investigations of plant stresses response mechanism are the focus area of research for plant scientists. Although these efforts lead to reveal different plant response mechanisms against salt stress, yet many questions still need to be answered to get a clear picture of plant strategy to cope with salt stress. Moreover, these studies have indicated the presence of a complicated network of different integrated pathways. In order to work in a progressive way, a review of current knowledge is critical. Therefore, this review aims to provide an overview of our understanding of plant response to salt stress and to indicate some important yet unexplored dynamics to improve our knowledge that could ultimately lead towards crop improvement.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Qin, F., Shinozaki, K., & Yamaguchi-Shinozaki, K. (2011). Achievements and challenges in understanding plant abiotic stress responses and tolerance. Plant and Cell Physiology, 52(9), 1569–1582. https://doi.org/10.1093/pcp/pcr106.

    Article  CAS  PubMed  Google Scholar 

  2. Shao, H.-B., Chu, L.-Y., Jaleel, C. A., & Zhao, C.-X. (2008). Water-deficit stress-induced anatomical changes in higher plants. Comptes Rendus Biologies, 331(3), 215–225. https://doi.org/10.1016/j.crvi.2008.01.002.

    Article  PubMed  Google Scholar 

  3. Munns, R., & Tester, M. (2008). Mechanisms of salinity tolerance. Annual Review of Plant Biology, 59(1), 651–681. https://doi.org/10.1146/annurev.arplant.59.032607.092911.

    Article  CAS  PubMed  Google Scholar 

  4. Gopal, S., Kim, K., Hu, S., & Sa, T. (2014). Effect of salinity on plants and the role of arbuscular mycorrhizal fungi and plant growth-promoting Rhizobacteria in alleviation of salt stress. In P. Ahmad & M. R. Wani (Eds.), Physiological mechanisms and adaptation strategies in plants under changing environment (pp. 115–144). New York: Springer. https://doi.org/10.1007/978-1-4614-8591-9_6.

    Chapter  Google Scholar 

  5. Flexas, J., Bota, J., Loreto, F., Cornic, G., & Sharkey, T. D. (2004). Diffusive and metabolic limitations to photosynthesis under drought and salinity in C3 plants. Plant Biology, 6(03), 269–279.

    Article  CAS  PubMed  Google Scholar 

  6. Flexas, J., DIAZ-ESPEJO, A., GalmES, J., Kaldenhoff, R., Medrano, H., & RIBAS-CARBO, M. (2007). Rapid variations of mesophyll conductance in response to changes in CO2 concentration around leaves. Plant, Cell & Environment, 30(10), 1284–1298.

    Article  CAS  Google Scholar 

  7. Ashraf, M. (2004). Some important physiological selection criteria for salt tolerance in plants. Flora—Morphology, Distribution, Functional Ecology of Plants, 199(5), 361–376. https://doi.org/10.1078/0367-2530-00165.

    Article  Google Scholar 

  8. Hasegawa, P. M., Bressan, R. A., Zhu, J.-K., & Bohnert, H. J. (2000). Plant cellular and molecular responses to high salinity. Annual Review of Plant Physiology and Plant Molecular Biology, 51(1), 463–499. https://doi.org/10.1146/annurev.arplant.51.1.463.

    Article  CAS  PubMed  Google Scholar 

  9. Krishnamurthy, L., Serraj, R., Hash, C. T., Dakheel, A. J., & Reddy, B. V. S. (2007). Screening sorghum genotypes for salinity tolerant biomass production. Euphytica, 156(1–2), 15–24. https://doi.org/10.1007/s10681-006-9343-9.

    Article  Google Scholar 

  10. Chinnusamy, A. J. V. (2005). Understanding and improving salt tolerance in plants. Crop Science, 45(2), 437–448. https://doi.org/10.2135/cropsci2005.0437.

    Article  CAS  Google Scholar 

  11. Golldack, D., Lüking, I., & Yang, O. (2011). Plant tolerance to drought and salinity: stress regulating transcription factors and their functional significance in the cellular transcriptional network. Plant Cell Reports, 30(8), 1383–1391. https://doi.org/10.1007/s00299-011-1068-0.

    Article  CAS  PubMed  Google Scholar 

  12. Chinnusamy, V., & Zhu, J.-K. (2009). Epigenetic regulation of stress responses in plants. Current Opinion in Plant Biology, 12(2), 133–139. https://doi.org/10.1016/j.pbi.2008.12.006.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Anschütz, U., Becker, D., & Shabala, S. (2014). Going beyond nutrition: regulation of potassium homoeostasis as a common denominator of plant adaptive responses to environment. Journal of Plant Physiology, 171(9), 670–687. https://doi.org/10.1016/j.jplph.2014.01.009.

    Article  CAS  PubMed  Google Scholar 

  14. Angers, B., Castonguay, E., & Massicotte, R. (2010). Environmentally induced phenotypes and DNA methylation: how to deal with unpredictable conditions until the next generation and after. Molecular Ecology, 19(7), 1283–1295. https://doi.org/10.1111/j.1365-294X.2010.04580.x.

    Article  CAS  PubMed  Google Scholar 

  15. Madlung, A., & Comai, L. (2004). The effect of stress on genome regulation and structure. Annals of Botany, 94(4), 481–495. https://doi.org/10.1093/aob/mch172.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Vanyushin, B. F., & Ashapkin, V. V. (2011). DNA methylation in higher plants: past, present and future. Biochimica et Biophysica Acta (BBA)—Gene Regulatory Mechanisms, 1809(8), 360–368. https://doi.org/10.1016/j.bbagrm.2011.04.006.

    Article  CAS  Google Scholar 

  17. Hirayama, T., & Shinozaki, K. (2010). Research on plant abiotic stress responses in the post-genome era: past, present and future. The Plant Journal, 61(6), 1041–1052. https://doi.org/10.1111/j.1365-313X.2010.04124.x.

    Article  CAS  PubMed  Google Scholar 

  18. Khan, M. S., Ahmad, D., & Khan, M. A. (2015). Trends in genetic engineering of plants with (Na+/H+) antiporters for salt stress tolerance. Biotechnology & Biotechnological Equipment, 29(5), 815–825.

    Article  CAS  Google Scholar 

  19. Zhang, H., Zhang, Q., Zhai, H., Li, Y., Wang, X., Liu, Q., & He, S. (2017). Transcript profile analysis reveals important roles of jasmonic acid signalling pathway in the response of sweet potato to salt stress. Scientific Reports, 7, 40819.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Gilroy, S., Suzuki, N., Miller, G., Choi, W.-G., Toyota, M., Devireddy, A. R., & Mittler, R. (2014). A tidal wave of signals: calcium and ROS at the forefront of rapid systemic signaling. Trends in Plant Science, 19(10), 623–630.

    Article  CAS  PubMed  Google Scholar 

  21. Zandalinas, S. I., Mittler, R., Balfagón, D., Arbona, V., & Gómez-Cadenas, A. (2018). Plant adaptations to the combination of drought and high temperatures. Physiologia Plantarum, 162(1), 2–12.

    Article  CAS  PubMed  Google Scholar 

  22. Casaretto, J. A., El-kereamy, A., Zeng, B., Stiegelmeyer, S. M., Chen, X., Bi, Y.-M., & Rothstein, S. J. (2016). Expression of OsMYB55 in maize activates stress-responsive genes and enhances heat and drought tolerance. BMC Genomics, 17(1), 312.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Awlia, M., Nigro, A., Fajkus, J., Schmoeckel, S. M., Negrão, S., Santelia, D., et al. (2016). High-throughput non-destructive phenotyping of traits that contribute to salinity tolerance in Arabidopsis thaliana. Frontiers in Plant Science, 7, 1414.

    Article  PubMed  PubMed Central  Google Scholar 

  24. Roy, S. J., Negrão, S., & Tester, M. (2014). Salt resistant crop plants. Current Opinion in Biotechnology, 26, 115–124.

    Article  CAS  PubMed  Google Scholar 

  25. Rajendran, K., Tester, M., & Roy, S. J. (2009). Quantifying the three main components of salinity tolerance in cereals. Plant, Cell & Environment, 32(3), 237–249.

    Article  CAS  Google Scholar 

  26. Berger, B., de Regt, B., & Tester, M. (2012). Trait dissection of salinity tolerance with plant phenomics. In Plant salt tolerance (pp. 399–413). Springer.

  27. Urao, T., Yakubov, B., Satoh, R., Yamaguchi-Shinozaki, K., Seki, M., Hirayama, T., & Shinozaki, K. (1999). A transmembrane hybrid-type histidine kinase in Arabidopsis functions as an osmosensor. The Plant Cell, 11(9), 1743–1754.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Tran, L.-S. P., Urao, T., Qin, F., Maruyama, K., Kakimoto, T., Shinozaki, K., & Yamaguchi-Shinozaki, K. (2007). Functional analysis of AHK1/ATHK1 and cytokinin receptor histidine kinases in response to abscisic acid, drought, and salt stress in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America, 104(51), 20623–20628. https://doi.org/10.1073/pnas.0706547105.

    Article  PubMed  PubMed Central  Google Scholar 

  29. Wohlbach, D. J., Quirino, B. F., & Sussman, M. R. (2008). Analysis of the Arabidopsis histidine kinase ATHK1 reveals a connection between vegetative osmotic stress sensing and seed maturation. The Plant Cell, 20(4), 1101–1117. https://doi.org/10.1105/tpc.107.055871.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Kumar, M. N., Jane, W.-N., & Verslues, P. E. (2013). Role of the putative osmosensor Arabidopsis histidine kinase1 in dehydration avoidance and low-water-potential response. Plant Physiology, 161(2), 942–953. https://doi.org/10.1104/pp.112.209791.

    Article  CAS  PubMed  Google Scholar 

  31. Deinlein, U., Stephan, A. B., Horie, T., Luo, W., Xu, G., & Schroeder, J. I. (2014). Plant salt-tolerance mechanisms. Trends in Plant Science, 19(6), 371–379. https://doi.org/10.1016/j.tplants.2014.02.001.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Zhu, J. K. (2001). Plant salt tolerance. Trends in Plant Science, 6(2), 66–71.

    Article  CAS  PubMed  Google Scholar 

  33. Tracy, F. E., Gilliham, M., Dodd, A. N., Webb, A. A. R., & Tester, M. (2008). NaCl-induced changes in cytosolic free Ca2+ in Arabidopsis thaliana are heterogeneous and modified by external ionic composition. Plant, Cell & Environment, 31(8), 1063–1073. https://doi.org/10.1111/j.1365-3040.2008.01817.x.

    Article  CAS  Google Scholar 

  34. López-Pérez, L., del Carmen Martínez-Ballesta, M., Maurel, C., & Carvajal, M. (2009). Changes in plasma membrane lipids, aquaporins and proton pump of broccoli roots, as an adaptation mechanism to salinity. Phytochemistry, 70(4), 492–500.

    Article  CAS  PubMed  Google Scholar 

  35. Scandalios, J. G. (2005). Oxidative stress: molecular perception and transduction of signals triggering antioxidant gene defenses. Brazilian Journal of Medical and Biological Research, 38(7), 995–1014.

    Article  CAS  PubMed  Google Scholar 

  36. Moore, C. A., Bowen, H. C., Scrase-Field, S., Knight, M. R., & White, P. J. (2002). The deposition of suberin lamellae determines the magnitude of cytosolic Ca2+ elevations in root endodermal cells subjected to cooling. The Plant Journal, 30(4), 457–465.

    Article  CAS  PubMed  Google Scholar 

  37. Luan, S., Kudla, J., Rodriguez-Concepcion, M., Yalovsky, S., & Gruissem, W. (2002). Calmodulins and calcineurin B-like proteins. The Plant Cell, 14(Suppl), s389–s400. https://doi.org/10.1105/tpc.001115.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Kiegle, E., Moore, C. A., Haseloff, J., Tester, M. A., & Knight, M. R. (2000). Cell-type-specific calcium responses to drought, salt and cold in the Arabidopsis root. The Plant Journal: For Cell and Molecular Biology, 23(2), 267–278.

    Article  CAS  Google Scholar 

  39. Cheong, Y. H., Kim, K.-N., Pandey, G. K., Gupta, R., Grant, J. J., & Luan, S. (2003). CBL1, a calcium sensor that differentially regulates salt, drought, and cold responses in Arabidopsis. The Plant Cell, 15(8), 1833–1845.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Gilroy, S., & Trewavas, A. (2001). Signal processing and transduction in plant cells: the end of the beginning? Nature Reviews Molecular Cell Biology, 2(4), 307–314. https://doi.org/10.1038/35067109.

    Article  CAS  PubMed  Google Scholar 

  41. Cornic, G., & Massacci, A. (1996). Leaf photosynthesis under drought stress. In Photosynthesis and the environment (pp. 347–366). Springer.

  42. Kasuga, M., Liu, Q., Miura, S., Yamaguchi-Shinozaki, K., & Shinozaki, K. (1999). Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nature Biotechnology, 17(3), 287.

    Article  CAS  PubMed  Google Scholar 

  43. Mahajan, S., & Tuteja, N. (2005). Cold, salinity and drought stresses: an overview. Archives of Biochemistry and Biophysics, 444(2), 139–158. https://doi.org/10.1016/j.abb.2005.10.018.

    Article  CAS  PubMed  Google Scholar 

  44. Xiong, L., & Zhu, J.-K. (2002). Molecular and genetic aspects of plant responses to osmotic stress. Plant, Cell & Environment, 25(2), 131–139.

    Article  CAS  Google Scholar 

  45. Zhu, J.-K. (2002). Salt and drought stress signal transduction in plants. Annual Review of Plant Biology, 53, 247–273. https://doi.org/10.1146/annurev.arplant.53.091401.143329.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Pei, Z.-M., Murata, Y., Benning, G., Thomine, S., Klüsener, B., Allen, G. J., et al. (2000). Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature, 406(6797), 731.

    Article  CAS  PubMed  Google Scholar 

  47. Zhang, X., Zhang, L., Dong, F., Gao, J., Galbraith, D. W., & Song, C.-P. (2001). Hydrogen peroxide is involved in abscisic acid-induced stomatal closure in Vicia faba. Plant Physiology, 126(4), 1438–1448.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Guan, L. M., Zhao, J., & Scandalios, J. G. (2000). Cis-elements and trans-factors that regulate expression of the maize Cat1 antioxidant gene in response to ABA and osmotic stress: H2O2 is the likely intermediary signaling molecule for the response. The Plant Journal, 22(2), 87–95. https://doi.org/10.1046/j.1365-313x.2000.00723.x.

    Article  CAS  PubMed  Google Scholar 

  49. Zhao, Z., Chen, G., & Zhang, C. (2001). Interaction between reactive oxygen species and nitric oxide in drought-induced abscisic acid synthesis in root tips of wheat seedlings. Functional Plant Biology, 28(10), 1055–1061.

    Article  CAS  Google Scholar 

  50. Murata, Y., Pei, Z.-M., Mori, I. C., & Schroeder, J. (2001). Abscisic acid activation of plasma membrane Ca2+ channels in guard cells requires cytosolic NAD (P) H and is differentially disrupted upstream and downstream of reactive oxygen species production in abi1-1 and abi2-1 protein phosphatase 2C mutants. The Plant Cell, 13(11), 2513–2523.

    CAS  PubMed  PubMed Central  Google Scholar 

  51. Yan, J., Tsuichihara, N., Etoh, T., & Iwai, S. (2007). Reactive oxygen species and nitric oxide are involved in ABA inhibition of stomatal opening. Plant, Cell & Environment, 30(10), 1320–1325.

    Article  CAS  Google Scholar 

  52. Price, A. H., Taylor, A., Ripley, S. J., Griffiths, A., Trewavas, A. J., & Knight, M. R. (1994). Oxidative signals in tobacco increase cytosolic calcium. The Plant Cell, 6(9), 1301–1310.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Chen, C.-W., Yang, Y.-W., Lur, H.-S., Tsai, Y.-G., & Chang, M.-C. (2006). A novel function of abscisic acid in the regulation of rice (Oryza sativa L.) root growth and development. Plant and Cell Physiology, 47(1), 1–13. https://doi.org/10.1093/pcp/pci216.

    Article  CAS  PubMed  Google Scholar 

  54. Park, H.-Y., Seok, H.-Y., Park, B.-K., Kim, S.-H., Goh, C.-H., Lee, B., et al. (2008). Overexpression of Arabidopsis ZEP enhances tolerance to osmotic stress. Biochemical and Biophysical Research Communications, 375(1), 80–85. https://doi.org/10.1016/j.bbrc.2008.07.128.

    Article  CAS  PubMed  Google Scholar 

  55. Cutler, S. R., Rodriguez, P. L., Finkelstein, R. R., & Abrams, S. R. (2010). Abscisic acid: emergence of a core signaling network. Annual Review of Plant Biology, 61, 651–679.

    Article  CAS  PubMed  Google Scholar 

  56. Zhang, J., Jia, W., Yang, J., & Ismail, A. M. (2006). Role of ABA in integrating plant responses to drought and salt stresses. Field Crops Research, 97(1), 111–119. https://doi.org/10.1016/j.fcr.2005.08.018.

    Article  Google Scholar 

  57. Xiong, L., & Zhu, J.-K. (2003). Regulation of abscisic acid biosynthesis. Plant Physiology, 133(1), 29–36.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Zhang, J., Yu, H., Zhang, Y., Wang, Y., Li, M., Zhang, J., … Li, Z. (2016). Increased abscisic acid levels in transgenic maize overexpressing AtLOS5 mediated root ion fluxes and leaf water status under salt stress. Journal of Experimental Botany, erv528. doi:https://doi.org/10.1093/jxb/erv528.

  59. Wang, F., Zhu, H., Chen, D., Li, Z., Peng, R., & Yao, Q. (2016). A grape bHLH transcription factor gene, VvbHLH1, increases the accumulation of flavonoids and enhances salt and drought tolerance in transgenic Arabidopsis thaliana. Plant Cell, Tissue and Organ Culture (PCTOC), 125(2), 387–398.

    Article  CAS  Google Scholar 

  60. Wang, F., Kong, W., Wong, G., Fu, L., Peng, R., Li, Z., & Yao, Q. (2016). AtMYB12 regulates flavonoids accumulation and abiotic stress tolerance in transgenic Arabidopsis thaliana. Molecular Genetics and Genomics, 291(4), 1545–1559.

    Article  CAS  PubMed  Google Scholar 

  61. Luo, J., Tang, S., Mei, F., Peng, X., Li, J., Li, X., et al. (2017). BnSIP1-1, a trihelix family gene, mediates abiotic stress tolerance and ABA signaling in Brassica napus. Frontiers in Plant Science, 8, 44.

    PubMed  PubMed Central  Google Scholar 

  62. Qian, Z.-J., Song, J.-J., Chaumont, F., & Ye, Q. (2015). Differential responses of plasma membrane aquaporins in mediating water transport of cucumber seedlings under osmotic and salt stresses. Plant, Cell & Environment, 38(3), 461–473. https://doi.org/10.1111/pce.12319.

    Article  CAS  Google Scholar 

  63. De Costa, W., Zörb, C., Hartung, W., & Schubert, S. (2007). Salt resistance is determined by osmotic adjustment and abscisic acid in newly developed maize hybrids in the first phase of salt stress. Physiologia Plantarum, 131(2), 311–321. https://doi.org/10.1111/j.1399-3054.2007.00962.x.

    Article  CAS  PubMed  Google Scholar 

  64. Kasahara, H., Hanada, A., Kuzuyama, T., Takagi, M., Kamiya, Y., & Yamaguchi, S. (2002). Contribution of the mevalonate and methylerythritol phosphate pathways to the biosynthesis of gibberellins in Arabidopsis. Journal of Biological Chemistry, 277(47), 45188–45194.

    Article  CAS  PubMed  Google Scholar 

  65. Colebrook, E. H., Thomas, S. G., Phillips, A. L., & Hedden, P. (2014). The role of gibberellin signalling in plant responses to abiotic stress. Journal of Experimental Biology, 217(1), 67–75. https://doi.org/10.1242/jeb.089938.

    Article  CAS  PubMed  Google Scholar 

  66. Hedden, P., & Thomas, S. G. (2012). Gibberellin biosynthesis and its regulation. Biochemical Journal, 444(1), 11–25.

    Article  CAS  PubMed  Google Scholar 

  67. O’Neill, D. P., Davidson, S. E., Clarke, V. C., Yamauchi, Y., Yamaguchi, S., Kamiya, Y., et al. (2010). Regulation of the gibberellin pathway by auxin and DELLA proteins. Planta, 232(5), 1141–1149.

    Article  CAS  PubMed  Google Scholar 

  68. Thomas, S. G., Phillips, A. L., & Hedden, P. (1999). Molecular cloning and functional expression of gibberellin 2-oxidases, multifunctional enzymes involved in gibberellin deactivation. Proceedings of the National Academy of Sciences, 96(8), 4698–4703.

    Article  CAS  Google Scholar 

  69. Weston, D. E., Elliott, R. C., Lester, D. R., Rameau, C., Reid, J. B., Murfet, I. C., & Ross, J. J. (2008). The pea DELLA proteins LA and CRY are important regulators of gibberellin synthesis and root growth. Plant Physiology, 147(1), 199–205.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Golldack, D., Li, C., Mohan, H., & Probst, N. (2013). Gibberellins and abscisic acid signal crosstalk: living and developing under unfavorable conditions. Plant Cell Reports, 32(7), 1007–1016.

    Article  CAS  PubMed  Google Scholar 

  71. Ueguchi-Tanaka, M., Ashikari, M., Nakajima, M., Itoh, H., Katoh, E., Kobayashi, M., et al. (2005). GIBBERELLIN INSENSITIVE DWARF1 encodes a soluble receptor for gibberellin. Nature, 437(7059), 693.

    Article  CAS  PubMed  Google Scholar 

  72. Griffiths, J., Murase, K., Rieu, I., Zentella, R., Zhang, Z.-L., Powers, S. J., et al. (2006). Genetic characterization and functional analysis of the GID1 gibberellin receptors in Arabidopsis. The Plant Cell, 18(12), 3399–3414.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Feng, S., Martinez, C., Gusmaroli, G., Wang, Y., Zhou, J., Wang, F., et al. (2008). Coordinated regulation of Arabidopsis thaliana development by light and gibberellins. Nature, 451(7177), 475.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Achard, P., Cheng, H., De Grauwe, L., Decat, J., Schoutteten, H., Moritz, T., et al. (2006). Integration of plant responses to environmentally activated phytohormonal signals. Science, 311(5757), 91–94.

    Article  CAS  PubMed  Google Scholar 

  75. Tyler, L., Thomas, S. G., Hu, J., Dill, A., Alonso, J. M., Ecker, J. R., & Sun, T. (2004). DELLA proteins and gibberellin-regulated seed germination and floral development in Arabidopsis. Plant Physiology, 135(2), 1008–1019.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Yu, H., Ito, T., Zhao, Y., Peng, J., Kumar, P., & Meyerowitz, E. M. (2004). Floral homeotic genes are targets of gibberellin signaling in flower development. Proceedings of the National Academy of Sciences of the United States of America, 101(20), 7827–7832. https://doi.org/10.1073/pnas.0402377101.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Silverstone, A. L., Jung, H.-S., Dill, A., Kawaide, H., Kamiya, Y., & Sun, T. (2001). Repressing a repressor: gibberellin-induced rapid reduction of the RGA protein in Arabidopsis. The Plant Cell, 13(7), 1555–1566.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Fu, X., Richards, D. E., Ait-Ali, T., Hynes, L. W., Ougham, H., Peng, J., & Harberd, N. P. (2002). Gibberellin-mediated proteasome-dependent degradation of the barley DELLA protein SLN1 repressor. The Plant Cell, 14(12), 3191–3200.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Sasaki, A., Itoh, H., Gomi, K., Ueguchi-Tanaka, M., Ishiyama, K., Kobayashi, M., et al. (2003). Accumulation of phosphorylated repressor for gibberellin signaling in an F-box mutant. Science, 299(5614), 1896–1898.

    Article  CAS  PubMed  Google Scholar 

  80. Dill, A., Thomas, S. G., Hu, J., Steber, C. M., & Sun, T. (2004). The Arabidopsis F-box protein SLEEPY1 targets gibberellin signaling repressors for gibberellin-induced degradation. The Plant Cell, 16(6), 1392–1405.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Achard, P., Gong, F., Cheminant, S., Alioua, M., Hedden, P., & Genschik, P. (2008). The cold-inducible CBF1 factor-dependent signaling pathway modulates the accumulation of the growth-repressing DELLA proteins via its effect on gibberellin metabolism. The Plant Cell, 20(8), 2117–2129. https://doi.org/10.1105/tpc.108.058941.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Ariizumi, T., Hauvermale, A. L., Nelson, S. K., Hanada, A., Yamaguchi, S., & Steber, C. M. (2013). Lifting DELLA repression of Arabidopsis seed germination by nonproteolytic gibberellin signaling. Plant Physiology, 162(4), 2125–2139.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Zentella, R., Zhang, Z.-L., Park, M., Thomas, S. G., Endo, A., Murase, K., et al. (2007). Global analysis of DELLA direct targets in early gibberellin signaling in Arabidopsis. The Plant Cell, 19(10), 3037–3057.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Ko, J.-H., Yang, S. H., & Han, K.-H. (2006). Upregulation of an Arabidopsis RING-H2 gene, XERICO, confers drought tolerance through increased abscisic acid biosynthesis. The Plant Journal, 47(3), 343–355. https://doi.org/10.1111/j.1365-313X.2006.02782.x.

    Article  CAS  PubMed  Google Scholar 

  85. Zeng, D.-E., Hou, P., Xiao, F., & Liu, Y. (2015). Overexpression of Arabidopsis XERICO gene confers enhanced drought and salt stress tolerance in rice (Oryza sativa L.) Journal of Plant Biochemistry and Biotechnology, 24(1), 56–64.

    Article  CAS  Google Scholar 

  86. Kazan, K. (2015). Diverse roles of jasmonates and ethylene in abiotic stress tolerance. Trends in Plant Science, 20(4), 219–229.

    Article  CAS  PubMed  Google Scholar 

  87. Riemann, M., Dhakarey, R., Hazman, M., Miro, B., Kohli, A., & Nick, P. (2015). Exploring jasmonates in the hormonal network of drought and salinity responses. Frontiers in Plant Science, 6, 1077.

    Article  PubMed  PubMed Central  Google Scholar 

  88. Song, S., Qi, T., Wasternack, C., & Xie, D. (2014). Jasmonate signaling and crosstalk with gibberellin and ethylene. Current Opinion in Plant Biology, 21, 112–119.

    Article  CAS  PubMed  Google Scholar 

  89. Boter, M., Ruíz-Rivero, O., Abdeen, A., & Prat, S. (2004). Conserved MYC transcription factors play a key role in jasmonate signaling both in tomato and Arabidopsis. Genes & Development, 18(13), 1577–1591.

    Article  CAS  Google Scholar 

  90. Hou, X., Lee, L. Y. C., Xia, K., Yan, Y., & Yu, H. (2010). DELLAs modulate jasmonate signaling via competitive binding to JAZs. Developmental Cell, 19(6), 884–894.

    Article  CAS  PubMed  Google Scholar 

  91. Wild, M., Davière, J.-M., Cheminant, S., Regnault, T., Baumberger, N., Heintz, D., et al. (2012). The Arabidopsis DELLA RGA-LIKE3 is a direct target of MYC2 and modulates jasmonate signaling responses. The Plant Cell, 24(8), 3307–3319.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Abeles, F. B., Morgan, P. W., & Saltveit Jr, M. E. (2012). Ethylene in plant biology. Academic Press.

  93. Jiang, C., Belfield, E. J., Cao, Y., Smith, J. A. C., & Harberd, N. P. (2013). An Arabidopsis soil-salinity–tolerance mutation confers ethylene-mediated enhancement of sodium/potassium homeostasis. The Plant Cell Online, 25(9), 3535–3552. https://doi.org/10.1105/tpc.113.115659.

    Article  CAS  Google Scholar 

  94. Peng, J., Li, Z., Wen, X., Li, W., Shi, H., Yang, L., et al. (2014). Salt-induced stabilization of EIN3/EIL1 confers salinity tolerance by deterring ROS accumulation in Arabidopsis. PLoS Genetics, 10(10), e1004664.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Wang, N. N., Shih, M.-C., & Li, N. (2005). The GUS reporter-aided analysis of the promoter activities of Arabidopsis ACC synthase genes AtACS4, AtACS5, and AtACS7 induced by hormones and stresses. Journal of Experimental Botany, 56(413), 909–920.

    Article  CAS  PubMed  Google Scholar 

  96. Li, G., Meng, X., Wang, R., Mao, G., Han, L., Liu, Y., & Zhang, S. (2012). Dual-level regulation of ACC synthase activity by MPK3/MPK6 cascade and its downstream WRKY transcription factor during ethylene induction in Arabidopsis. PLoS Genetics, 8(6), e1002767.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Wang, K. L.-C., Li, H., & Ecker, J. R. (2002). Ethylene biosynthesis and signaling networks. The Plant Cell, 14(suppl 1), S131–S151.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Shen, X., Wang, Z., Song, X., Xu, J., Jiang, C., Zhao, Y., et al. (2014). Transcriptomic profiling revealed an important role of cell wall remodeling and ethylene signaling pathway during salt acclimation in Arabidopsis. Plant Molecular Biology, 86(3), 303–317.

    Article  CAS  PubMed  Google Scholar 

  99. CAO, W.-H., Liu, J., ZHOU, Q.-Y., CAO, Y.-R., ZHENG, S.-F., DU, B.-X., … CHEN, S.-Y. (2006). Expression of tobacco ethylene receptor NTHK1 alters plant responses to salt stress. Plant, Cell & Environment, 29(7), 1210–1219.

    Article  CAS  Google Scholar 

  100. Peng, Z., He, S., Gong, W., Sun, J., Pan, Z., Xu, F., et al. (2014). Comprehensive analysis of differentially expressed genes and transcriptional regulation induced by salt stress in two contrasting cotton genotypes. BMC Genomics, 15(1), 760.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Kukreja, S., Nandwal, A. S., Kumar, N., Sharma, S. K., Unvi, V., & Sharma, P. K. (2005). Plant water status, H 2 O 2 scavenging enzymes, ethylene evolution and membrane integrity of Cicer arietinum roots as affected by salinity. Biologia Plantarum, 49(2), 305–308.

    Article  CAS  Google Scholar 

  102. Tao, J.-J., Chen, H.-W., Ma, B., Zhang, W.-K., Chen, S.-Y., & Zhang, J.-S. (2015). The role of ethylene in plants under salinity stress. Frontiers in Plant Science, 6, 1059.

    Article  PubMed  PubMed Central  Google Scholar 

  103. Ali, S., Charles, T. C., & Glick, B. R. (2014). Amelioration of high salinity stress damage by plant growth-promoting bacterial endophytes that contain ACC deaminase. Plant Physiology and Biochemistry, 80, 160–167.

    Article  CAS  PubMed  Google Scholar 

  104. Barnawal, D., Bharti, N., Maji, D., Chanotiya, C. S., & Kalra, A. (2014). ACC deaminase-containing Arthrobacter protophormiae induces NaCl stress tolerance through reduced ACC oxidase activity and ethylene production resulting in improved nodulation and mycorrhization in Pisum sativum. Journal of Plant Physiology, 171(11), 884–894.

    Article  CAS  PubMed  Google Scholar 

  105. Chen, D., Ma, X., Li, C., Zhang, W., Xia, G., & Wang, M. (2014). A wheat aminocyclopropane-1-carboxylate oxidase gene, TaACO1, negatively regulates salinity stress in Arabidopsis thaliana. Plant Cell Reports, 33(11), 1815–1827.

    Article  CAS  PubMed  Google Scholar 

  106. Dong, H., Zhen, Z., Peng, J., Chang, L., Gong, Q., & Wang, N. N. (2011). Loss of ACS7 confers abiotic stress tolerance by modulating ABA sensitivity and accumulation in Arabidopsis. Journal of Experimental Botany, 62(14), 4875–4887.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Kim, K., Park, S.-H., Chae, J.-C., Soh, B. Y., & Lee, K.-J. (2014). Rapid degradation of Pseudomonas fluorescens 1-aminocyclopropane-1-carboxylic acid deaminase proteins expressed in transgenic Arabidopsis. FEMS Microbiology Letters, 355(2), 193–200.

    Article  CAS  PubMed  Google Scholar 

  108. Li, C.-H., Wang, G., Zhao, J.-L., Zhang, L.-Q., Ai, L.-F., Han, Y.-F., et al. (2014). The receptor-like kinase SIT1 mediates salt sensitivity by activating MAPK3/6 and regulating ethylene homeostasis in rice. The Plant Cell, 26(6), 2538–2553.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Xu, J., Li, Y., Wang, Y., Liu, H., Lei, L., Yang, H., et al. (2008). Activation of MAPK kinase 9 induces ethylene and camalexin biosynthesis and enhances sensitivity to salt stress in Arabidopsis. Journal of Biological Chemistry, 283(40), 26996–27006.

    Article  CAS  PubMed  Google Scholar 

  110. Christians, M. J., Gingerich, D. J., Hansen, M., Binder, B. M., Kieber, J. J., & Vierstra, R. D. (2009). The BTB ubiquitin ligases ETO1, EOL1 and EOL2 act collectively to regulate ethylene biosynthesis in Arabidopsis by controlling type-2 ACC synthase levels. The Plant Journal, 57(2), 332–345.

    Article  CAS  PubMed  Google Scholar 

  111. Du, H., Wu, N., Cui, F., You, L., Li, X., & Xiong, L. (2014). A homolog of ETHYLENE OVERPRODUCER, OsETOL1, differentially modulates drought and submergence tolerance in rice. The Plant Journal, 78(5), 834–849.

    Article  CAS  PubMed  Google Scholar 

  112. Foreman, J., Demidchik, V., Bothwell, J. H., Mylona, P., Miedema, H., Torres, M. A., et al. (2003). Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature, 422(6930), 442.

    Article  CAS  PubMed  Google Scholar 

  113. Bose, J., Rodrigo-Moreno, A., & Shabala, S. (2014). ROS homeostasis in halophytes in the context of salinity stress tolerance. Journal of Experimental Botany, 65(5), 1241–1257.

    Article  CAS  PubMed  Google Scholar 

  114. Jiang, C., Belfield, E. J., Mithani, A., Visscher, A., Ragoussis, J., Mott, R., et al. (2012). ROS-mediated vascular homeostatic control of root-to-shoot soil Na delivery in Arabidopsis. The EMBO Journal, 31(22), 4359–4370.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Wu, L., Zhang, Z., Zhang, H., Wang, X.-C., & Huang, R. (2008). Transcriptional modulation of ethylene response factor protein JERF3 in the oxidative stress response enhances tolerance of tobacco seedlings to salt, drought, and freezing. Plant Physiology, 148(4), 1953–1963.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Tanaka, Y., Sano, T., Tamaoki, M., Nakajima, N., Kondo, N., & Hasezawa, S. (2005). Ethylene inhibits abscisic acid-induced stomatal closure in Arabidopsis. Plant Physiology, 138(4), 2337–2343.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Suhita, D., Raghavendra, A. S., Kwak, J. M., & Vavasseur, A. (2004). Cytoplasmic alkalization precedes reactive oxygen species production during methyl jasmonate-and abscisic acid-induced stomatal closure. Plant Physiology, 134(4), 1536–1545.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Tester, M., & Davenport, R. (2003). Na+ tolerance and Na+ transport in higher plants. Annals of Botany, 91(5), 503–527.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Ji, H., Pardo, J. M., Batelli, G., Van Oosten, M. J., Bressan, R. A., & Li, X. (2013). The salt overly sensitive (SOS) pathway: established and emerging roles. Molecular Plant, 6(2), 275–286. https://doi.org/10.1093/mp/sst017.

    Article  CAS  PubMed  Google Scholar 

  120. Munns, R. (2002). Comparative physiology of salt and water stress. Plant, Cell & Environment, 25(2), 239–250.

    Article  CAS  Google Scholar 

  121. Olias, R., Eljakaoui, Z., Li, J. U. N., DE MORALES, P. A., MARÍN-MANZANO, M. C., Pardo, J. M., & Belver, A. (2009). The plasma membrane Na+/H+ antiporter SOS1 is essential for salt tolerance in tomato and affects the partitioning of Na+ between plant organs. Plant, Cell & Environment, 32(7), 904–916.

    Article  Google Scholar 

  122. Zhu, J.-K., Liu, J., & Xiong, L. (1998). Genetic analysis of salt tolerance in Arabidopsis: evidence for a critical role of potassium nutrition. The Plant Cell, 10(7), 1181–1191. https://doi.org/10.2307/3870720.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. Kopittke, P. M. (2012). Interactions between Ca, Mg, Na and K: alleviation of toxicity in saline solutions. Plant and Soil, 352(1–2), 353–362.

    Article  CAS  Google Scholar 

  124. Pyo, Y. J., Gierth, M., Schroeder, J. I., & Cho, M. H. (2010). High-affinity K+ transport in Arabidopsis: AtHAK5 and AKT1 are vital for seedling establishment and postgermination growth under low-potassium conditions. Plant Physiology, 153(2), 863–875.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Qi, Z., & Spalding, E. P. (2004). Protection of plasma membrane K+ transport by the salt overly sensitive1 Na+-H+ antiporter during salinity stress. Plant Physiology, 136(1), 2548–2555.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. Rus, A., Lee, B., Muñoz-Mayor, A., Sharkhuu, A., Miura, K., Zhu, J.-K., et al. (2004). AtHKT1 facilitates Na+ homeostasis and K+ nutrition in planta. Plant Physiology, 136(1), 2500–2511.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Rus, A., Yokoi, S., Sharkhuu, A., Reddy, M., Lee, B., Matsumoto, T. K., et al. (2001). AtHKT1 is a salt tolerance determinant that controls Na+ entry into plant roots. Proceedings of the National Academy of Sciences, 98(24), 14150–14155.

    Article  CAS  Google Scholar 

  128. Batelli, G., Verslues, P. E., Agius, F., Qiu, Q., Fujii, H., Pan, S., et al. (2007). SOS2 promotes salt tolerance in part by interacting with the vacuolar H+-ATPase and upregulating its transport activity. Molecular and Cellular Biology, 27(22), 7781–7790.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Krebs, M., Beyhl, D., Görlich, E., Al-Rasheid, K. A., Marten, I., Stierhof, Y.-D., et al. (2010). Arabidopsis V-ATPase activity at the tonoplast is required for efficient nutrient storage but not for sodium accumulation. Proceedings of the National Academy of Sciences, 107(7), 3251–3256.

    Article  Google Scholar 

  130. Oh, D.-H., Lee, S. Y., Bressan, R. A., Yun, D.-J., & Bohnert, H. J. (2010). Intracellular consequences of SOS1 deficiency during salt stress. Journal of Experimental Botany, 61(4), 1205–1213.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  131. Knight, H., Trewavas, A. J., & Knight, M. R. (1997). Calcium signalling in Arabidopsis thaliana responding to drought and salinity. The Plant Journal: For Cell and Molecular Biology, 12(5), 1067–1078.

    Article  CAS  Google Scholar 

  132. Martí, M. C., Stancombe, M. A., & Webb, A. A. R. (2013). Cell- and stimulus type-specific intracellular free Ca2+ signals in Arabidopsis. Plant Physiology, 163(2), 625–634. https://doi.org/10.1104/pp.113.222901.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  133. Kurusu, T., Kuchitsu, K., Nakano, M., Nakayama, Y., & Iida, H. (2013). Plant mechanosensing and Ca2+ transport. Trends in Plant Science, 18(4), 227–233. https://doi.org/10.1016/j.tplants.2012.12.002.

    Article  CAS  PubMed  Google Scholar 

  134. Yuan, F., Yang, H., Xue, Y., Kong, D., Ye, R., Li, C., et al. (2014). OSCA1 mediates osmotic-stress-evoked Ca 2+ increases vital for osmosensing in Arabidopsis. Nature, 514(7522), 367.

    Article  CAS  PubMed  Google Scholar 

  135. Im, J. H., Lee, H., Kim, J., Kim, H. B., & An, C. S. (2012). Soybean MAPK, GMK1 is dually regulated by phosphatidic acid and hydrogen peroxide and translocated to nucleus during salt stress. Molecules and Cells, 34(3), 271–278. https://doi.org/10.1007/s10059-012-0092-4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. Boudsocq, M., & Sheen, J. (2013). CDPKs in immune and stress signaling. Trends in Plant Science, 18(1), 30–40. https://doi.org/10.1016/j.tplants.2012.08.008.

    Article  CAS  PubMed  Google Scholar 

  137. Benn, G., Wang, C.-Q., Hicks, D. R., Stein, J., Guthrie, C., & Dehesh, K. (2014). A key general stress response motif is regulated non-uniformly by CAMTA transcription factors. The Plant Journal, 80(1), 82–92. https://doi.org/10.1111/tpj.12620.

    Article  CAS  PubMed  Google Scholar 

  138. Wang, M., Gu, D., Liu, T., Wang, Z., Guo, X., Hou, W., et al. (2007). Overexpression of a putative maize calcineurin B-like protein in Arabidopsis confers salt tolerance. Plant Molecular Biology, 65(6), 733–746. https://doi.org/10.1007/s11103-007-9238-8.

    Article  CAS  PubMed  Google Scholar 

  139. Tripathi, V., Parasuraman, B., Laxmi, A., & Chattopadhyay, D. (2009). CIPK6, a CBL-interacting protein kinase is required for development and salt tolerance in plants. The Plant Journal, 58(5), 778–790. https://doi.org/10.1111/j.1365-313X.2009.03812.x.

    Article  CAS  PubMed  Google Scholar 

  140. Moon, H., Lee, B., Choi, G., Shin, D., Prasad, D. T., Lee, O., et al. (2003). NDP kinase 2 interacts with two oxidative stress-activated MAPKs to regulate cellular redox state and enhances multiple stress tolerance in transgenic plants. Proceedings of the National Academy of Sciences of the United States of America, 100(1), 358–363. https://doi.org/10.1073/pnas.252641899.

    Article  CAS  PubMed  Google Scholar 

  141. Geng, Y., Wu, R., Wee, C. W., Xie, F., Wei, X., Chan, P. M. Y., et al. (2013). A spatio-temporal understanding of growth regulation during the salt stress response in Arabidopsis. The Plant Cell, 25(6), 2132–2154. https://doi.org/10.1105/tpc.113.112896.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  142. Chen, W., Provart, N. J., Glazebrook, J., Katagiri, F., Chang, H.-S., Eulgem, T., et al. (2002). Expression profile matrix of Arabidopsis transcription factor genes suggests their putative functions in response to environmental stresses. The Plant Cell, 14(3), 559–574.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  143. Duan, L., Dietrich, D., Ng, C. H., Chan, P. M. Y., Bhalerao, R., Bennett, M. J., & Dinneny, J. R. (2013). Endodermal ABA signaling promotes lateral root quiescence during salt stress in Arabidopsis seedlings. The Plant Cell, 25(1), 324–341. https://doi.org/10.1105/tpc.112.107227.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  144. Galvan-Ampudia, C. S., Julkowska, M. M., Darwish, E., Gandullo, J., Korver, R. A., Brunoud, G., et al. (2013). Halotropism is a response of plant roots to avoid a saline environment. Current Biology, 23(20), 2044–2050. https://doi.org/10.1016/j.cub.2013.08.042.

    Article  CAS  PubMed  Google Scholar 

  145. Chaves, M. M., & Oliveira, M. M. (2004). Mechanisms underlying plant resilience to water deficits: prospects for water-saving agriculture. Journal of Experimental Botany, 55(407), 2365–2384.

    Article  CAS  PubMed  Google Scholar 

  146. Dubouzet, J. G., Sakuma, Y., Ito, Y., Kasuga, M., Dubouzet, E. G., Miura, S., et al. (2003). OsDREB genes in rice, Oryza sativa L., encode transcription activators that function in drought-, high-salt- and cold-responsive gene expression. The Plant Journal, 33(4), 751–763. https://doi.org/10.1046/j.1365-313X.2003.01661.x.

    Article  CAS  PubMed  Google Scholar 

  147. Liu, J., & Zhu, J.-K. (1998). A calcium sensor homolog required for plant salt tolerance. Science, 280(5371), 1943–1945. https://doi.org/10.1126/science.280.5371.1943.

    Article  CAS  PubMed  Google Scholar 

  148. Yamaguchi-Shinozaki, K., & Shinozaki, K. (2006). Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annual Review of Plant Biology, 57(1), 781–803. https://doi.org/10.1146/annurev.arplant.57.032905.105444.

    Article  CAS  PubMed  Google Scholar 

  149. Jaglo-Ottosen, K. R., Gilmour, S. J., Zarka, D. G., Schabenberger, O., & Thomashow, M. F. (1998). Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. Science, 280(5360), 104–106. https://doi.org/10.1126/science.280.5360.104.

    Article  CAS  PubMed  Google Scholar 

  150. Shinozaki, K., & Yamaguchi-Shinozaki, K. (2000). Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways. Current Opinion in Plant Biology, 3(3), 217–223.

    Article  CAS  PubMed  Google Scholar 

  151. Thomashow, M. F. (2001). So what’s new in the field of plant cold acclimation? Lots! Plant Physiology, 125(1), 89–93.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  152. Urao, T., Yamaguchi-Shinozaki, K., & Shinozaki, K. (2000). Two-component systems in plant signal transduction. Trends in Plant Science, 5(2), 67–74.

    Article  CAS  PubMed  Google Scholar 

  153. Sakai, H., Aoyama, T., & Oka, A. (2000). Arabidopsis ARR1 and ARR2 response regulators operate as transcriptional activators. The Plant Journal, 24(6), 703–711.

    Article  CAS  PubMed  Google Scholar 

  154. Lohrmann, J., Sweere, U., Zabaleta, E., Baurle, I., Keitel, C., Kozma-Bognar, L., et al. (2001). The response regulator ARR2: a pollen-specific transcription factor involved in the expression of nuclear genes for components of mitochondrial complex I in Arabidopsis. Molecular Genetics and Genomics, 265(1), 2–13.

    Article  CAS  PubMed  Google Scholar 

  155. Patharkar, O. R., & Cushman, J. C. (2000). A stress-induced calcium-dependent protein kinase from Mesembryanthemum crystallinum phosphorylates a two-component pseudo-response regulator. The Plant Journal, 24(5), 679–691.

    Article  CAS  PubMed  Google Scholar 

  156. Sheen, J. (1996). Ca2+-dependent protein kinases and stress signal transduction in plants. Science, 274(5294), 1900–1902.

    Article  CAS  PubMed  Google Scholar 

  157. Liu, Q., Kasuga, M., Sakuma, Y., Abe, H., Miura, S., Yamaguchi-Shinozaki, K., & Shinozaki, K. (1998). Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis. The Plant Cell, 10(8), 1391–1406. https://doi.org/10.1105/tpc.10.8.1391.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  158. Nakashima, K., Shinwari, Z. K., Sakuma, Y., Seki, M., Miura, S., Shinozaki, K., & Yamaguchi-Shinozaki, K. (2000). Organization and expression of two Arabidopsis DREB2 genes encoding DRE-binding proteins involved in dehydration- and high-salinity-responsive gene expression. Plant Molecular Biology, 42(4), 657–665. https://doi.org/10.1023/A:1006321900483.

    Article  CAS  PubMed  Google Scholar 

  159. Qin, F., Kakimoto, M., Sakuma, Y., Maruyama, K., Osakabe, Y., Tran, L.-S. P., et al. (2007). Regulation and functional analysis of ZmDREB2A in response to drought and heat stresses in Zea mays L. The Plant Journal, 50(1), 54–69. https://doi.org/10.1111/j.1365-313X.2007.03034.x.

    Article  CAS  PubMed  Google Scholar 

  160. Sakuma, Y., Maruyama, K., Osakabe, Y., Qin, F., Seki, M., Shinozaki, K., & Yamaguchi-Shinozaki, K. (2006). Functional analysis of an Arabidopsis transcription factor, DREB2A, involved in drought-responsive gene expression. The Plant Cell, 18(5), 1292–1309. https://doi.org/10.1105/tpc.105.035881.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  161. Yang, A., Dai, X., & Zhang, W.-H. (2012). A R2R3-type MYB gene, OsMYB2, is involved in salt, cold, and dehydration tolerance in rice. Journal of Experimental Botany, 63(7), 2541–2556. https://doi.org/10.1093/jxb/err431.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  162. Shen, X., Guo, X., Guo, X., Zhao, D., Zhao, W., Chen, J., & Li, T. (2017). PacMYBA, a sweet cherry R2R3-MYB transcription factor, is a positive regulator of salt stress tolerance and pathogen resistance. Plant Physiology and Biochemistry, 112, 302–311.

    Article  CAS  PubMed  Google Scholar 

  163. Kim, I.-S., Sinha, S., De Crombrugghe, B., & Maity, S. N. (1996). Determination of functional domains in the C subunit of the CCAAT-binding factor (CBF) necessary for formation of a CBF-DNA complex: CBF-B interacts simultaneously with both the CBF-A and CBF-C subunits to form a heterotrimeric CBF molecule. Molecular and Cellular Biology, 16(8), 4003–4013.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  164. Chen, N.-Z., Zhang, X.-Q., Wei, P.-C., Chen, Q.-J., Ren, F., Chen, J., & Wang, X.-C. (2007). AtHAP3b plays a crucial role in the regulation of flowering time in Arabidopsis during osmotic stress. BMB Reports, 40(6), 1083–1089.

    Article  CAS  Google Scholar 

  165. Li, W.-X., Oono, Y., Zhu, J., He, X.-J., Wu, J.-M., Iida, K., et al. (2008). The Arabidopsis NFYA5 transcription factor is regulated transcriptionally and posttranscriptionally to promote drought resistance. The Plant Cell, 20(8), 2238–2251.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  166. Nelson, D. E., Repetti, P. P., Adams, T. R., Creelman, R. A., Wu, J., Warner, D. C., et al. (2007). Plant nuclear factor Y (NF-Y) B subunits confer drought tolerance and lead to improved corn yields on water-limited acres. Proceedings of the National Academy of Sciences, 104(42), 16450–16455.

    Article  Google Scholar 

  167. Zhao, B., Ge, L., Liang, R., Li, W., Ruan, K., Lin, H., & Jin, Y. (2009). Members of miR-169 family are induced by high salinity and transiently inhibit the NF-YA transcription factor. BMC Molecular Biology, 10(1), 29.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  168. Hackenberg, D., Keetman, U., & Grimm, B. (2012). Homologous NF-YC2 subunit from Arabidopsis and tobacco is activated by photooxidative stress and induces flowering. International Journal of Molecular Sciences, 13(3), 3458–3477.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  169. Li, Y.-J., Fang, Y., Fu, Y.-R., Huang, J.-G., Wu, C.-A., & Zheng, C.-C. (2013). NFYA1 is involved in regulation of postgermination growth arrest under salt stress in Arabidopsis. PLoS One, 8(4), e61289.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  170. Ni, Z., Hu, Z., Jiang, Q., & Zhang, H. (2013). GmNFYA3, a target gene of miR169, is a positive regulator of plant tolerance to drought stress. Plant Molecular Biology, 82(1–2), 113–129.

    Article  CAS  PubMed  Google Scholar 

  171. Yang, M., Zhao, Y., Shi, S., Du, X., Gu, J., & Xiao, K. (2017). Wheat nuclear factor Y (NF-Y) B subfamily gene TaNF-YB3; l confers critical drought tolerance through modulation of the ABA-associated signaling pathway. Plant Cell, Tissue and Organ Culture (PCTOC), 128(1), 97–111.

    Article  CAS  Google Scholar 

  172. Rizhsky, L., Liang, H., Shuman, J., Shulaev, V., Davletova, S., & Mittler, R. (2004). When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. Plant Physiology, 134(4), 1683–1696. https://doi.org/10.1104/pp.103.033431.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  173. Gu, L., Zhang, Y., Zhang, M., Li, T., Dirk, L. M. A., Downie, B., & Zhao, T. (2016). ZmGOLS2, a target of transcription factor ZmDREB2A, offers similar protection against abiotic stress as ZmDREB2A. Plant Molecular Biology, 90(1–2), 157–170. https://doi.org/10.1007/s11103-015-0403-1.

    Article  CAS  PubMed  Google Scholar 

  174. Ren, Z.-H., Gao, J.-P., Li, L.-G., Cai, X.-L., Huang, W., Chao, D.-Y., et al. (2005). A rice quantitative trait locus for salt tolerance encodes a sodium transporter. Nature Genetics, 37(10), 1141.

    Article  CAS  PubMed  Google Scholar 

  175. Munns, R., James, R. A., Xu, B., Athman, A., Conn, S. J., Jordans, C., et al. (2012). Wheat grain yield on saline soils is improved by an ancestral Na+ transporter gene. Nature Biotechnology, 30(4), 360.

    Article  CAS  PubMed  Google Scholar 

  176. Tiwari, S., Krishnamurthy, S. L., Kumar, V., Singh, B., Rao, A. R., Mithra, S. V. A., et al. (2016). Mapping QTLs for salt tolerance in rice (Oryza sativa L.) by bulked segregant analysis of recombinant inbred lines using 50K SNP chip. PLoS One, 11(4), e0153610.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  177. Luo, M., Zhao, Y., Zhang, R., Xing, J., Duan, M., Li, J., et al. (2017). Mapping of a major QTL for salt tolerance of mature field-grown maize plants based on SNP markers. BMC Plant Biology, 17(1), 140.

    Article  PubMed  PubMed Central  Google Scholar 

  178. Yang, W., Guo, Z., Huang, C., Duan, L., Chen, G., Jiang, N., et al. (2014). Combining high-throughput phenotyping and genome-wide association studies to reveal natural genetic variation in rice. Nature Communications, 5, 5087.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  179. Farazi, T. A., Juranek, S. A., & Tuschl, T. (2008). The growing catalog of small RNAs and their association with distinct Argonaute/Piwi family members. Development (Cambridge, England), 135(7), 1201–1214. https://doi.org/10.1242/dev.005629(OK).

    Article  CAS  Google Scholar 

  180. Navarro, L., Dunoyer, P., Jay, F., Arnold, B., Dharmasiri, N., Estelle, M., et al. (2006). A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science, 312(5772), 436–439 OK.

    Article  CAS  PubMed  Google Scholar 

  181. Sunkar, R., & Zhu, J.-K. (2004). Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. The Plant Cell, 16(8), 2001–2019 OK.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  182. Jagadeeswaran, G., Saini, A., & Sunkar, R. (2009). Biotic and abiotic stress down-regulate miR398 expression in Arabidopsis. Planta, 229(4), 1009–1014.

    Article  CAS  PubMed  Google Scholar 

  183. Liu, H.-H., Tian, X., Li, Y.-J., Wu, C.-A., & Zheng, C.-C. (2008). Microarray-based analysis of stress-regulated microRNAs in Arabidopsis thaliana. RNA (New York, N.Y.), 14(5), 836–843. doi:https://doi.org/10.1261/rna.895308.

  184. Chen, L., Wang, T., Zhao, M., Tian, Q., & Zhang, W.-H. (2012). Identification of aluminum-responsive microRNAs in Medicago truncatula by genome-wide high-throughput sequencing. Planta, 235(2), 375–386. https://doi.org/10.1007/s00425-011-1514-9.

    Article  CAS  PubMed  Google Scholar 

  185. Ben Amor, B., Wirth, S., Merchan, F., Laporte, P., d’Aubenton-Carafa, Y., Hirsch, J., et al. (2009). Novel long non-protein coding RNAs involved in Arabidopsis differentiation and stress responses. Genome Research, 19(1), 57–69. https://doi.org/10.1101/gr.080275.108.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  186. Kinoshita, N., Wang, H., Kasahara, H., Liu, J., Macpherson, C., Machida, Y., et al. (2012). IAA-Ala Resistant3, an evolutionarily conserved target of miR167, mediates Arabidopsis root architecture changes during high osmotic stress. The Plant Cell, 24(9), 3590–3602. https://doi.org/10.1105/tpc.112.097006.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  187. Jung, H. J., & Kang, H. (2007). Expression and functional analyses of microRNA417 in Arabidopsis thaliana under stress conditions. Plant Physiology and Biochemistry: PPB, 45(10–11), 805–811. https://doi.org/10.1016/j.plaphy.2007.07.015.

    Article  CAS  PubMed  Google Scholar 

  188. Wang, B., Sun, Y., Song, N., Wei, J., Wang, X., Feng, H., et al. (2014). MicroRNAs involving in cold, wounding and salt stresses in Triticum aestivum L. Plant Physiology and Biochemistry, 80, 90–96.

    Article  CAS  PubMed  Google Scholar 

  189. Lu, W., Li, J., Liu, F., Gu, J., Guo, C., Xu, L., et al. (2011). Expression pattern of wheat miRNAs under salinity stress and prediction of salt-inducible miRNAs targets. Frontiers of Agriculture in China, 5(4), 413–422. https://doi.org/10.1007/s11703-011-1133-z.

    Article  Google Scholar 

  190. Lu, S., Sun, Y.-H., & Chiang, V. L. (2008). Stress-responsive microRNAs in Populus. The Plant Journal: For Cell and Molecular Biology, 55(1), 131–151. https://doi.org/10.1111/j.1365-313X.2008.03497.x.

    Article  CAS  Google Scholar 

  191. Barrera-Figueroa, B. E., Gao, L., Wu, Z., Zhou, X., Zhu, J., Jin, H., et al. (2012). High throughput sequencing reveals novel and abiotic stress-regulated microRNAs in the inflorescences of rice. BMC Plant Biology, 12, 132. https://doi.org/10.1186/1471-2229-12-132.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  192. Jian, X., Zhang, L., Li, G., Zhang, L., Wang, X., Cao, X., et al. (2010). Identification of novel stress-regulated microRNAs from Oryza sativa L. Genomics, 95(1), 47–55. https://doi.org/10.1016/j.ygeno.2009.08.017.

    Article  CAS  PubMed  Google Scholar 

  193. Macovei, A., & Tuteja, N. (2012). microRNAs targeting DEAD-box helicases are involved in salinity stress response in rice (Oryza sativa L.) BMC Plant Biology, 12, 183. https://doi.org/10.1186/1471-2229-12-183.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  194. Gao, P., Bai, X., Yang, L., Lv, D., Li, Y., Cai, H., et al. (2010). Over-expression of osa-MIR396c decreases salt and alkali stress tolerance. Planta, 231(5), 991–1001. https://doi.org/10.1007/s00425-010-1104-2.

    Article  CAS  PubMed  Google Scholar 

  195. Gao, P., Bai, X., Yang, L., Lv, D., Pan, X., Li, Y., et al. (2011). osa-MIR393: a salinity- and alkaline stress-related microRNA gene. Molecular Biology Reports, 38(1), 237–242. https://doi.org/10.1007/s11033-010-0100-8.

    Article  CAS  PubMed  Google Scholar 

  196. Li, B., Duan, H., Li, J., Deng, X. W., Yin, W., & Xia, X. (2013). Global identification of miRNAs and targets in Populus euphratica under salt stress. Plant Molecular Biology, 81(6), 525–539.

    Article  CAS  PubMed  Google Scholar 

  197. Qin, Y., Duan, Z., Xia, X., & Yin, W. (2011). Expression profiles of precursor and mature microRNAs under dehydration and high salinity shock in Populus euphratica. Plant Cell Reports, 30(10), 1893–1907. https://doi.org/10.1007/s00299-011-1096-9.

    Article  CAS  PubMed  Google Scholar 

  198. Li, H., Dong, Y., Yin, H., Wang, N., Yang, J., Liu, X., et al. (2011). Characterization of the stress associated microRNAs in glycine max by deep sequencing. BMC Plant Biology, 11, 170. https://doi.org/10.1186/1471-2229-11-170.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  199. Arenas-Huertero, C., Pérez, B., Rabanal, F., Blanco-Melo, D., De la Rosa, C., Estrada-Navarrete, G., et al. (2009). Conserved and novel miRNAs in the legume Phaseolus vulgaris in response to stress. Plant Molecular Biology, 70(4), 385–401. https://doi.org/10.1007/s11103-009-9480-3.

    Article  CAS  PubMed  Google Scholar 

  200. Ding, D., Zhang, L., Wang, H., Liu, Z., Zhang, Z., & Zheng, Y. (2009). Differential expression of miRNAs in response to salt stress in maize roots. Annals of Botany, 103(1), 29–38. https://doi.org/10.1093/aob/mcn205.

    Article  CAS  PubMed  Google Scholar 

  201. Kong, Y., Elling, A. A., Chen, B., & Deng, X. (2010). Differential expression of microRNAs in maize inbred and hybrid lines during salt and drought stress. American Journal of Plant Sciences, 01(02), 69. https://doi.org/10.4236/ajps.2010.12009.

    Article  CAS  Google Scholar 

  202. Luan, M., Xu, M., Lu, Y., Zhang, L., Fan, Y., & Wang, L. (2015). Expression of zma-miR169 miRNAs and their target ZmNF-YA genes in response to abiotic stress in maize leaves. Gene, 555(2), 178–185. https://doi.org/10.1016/j.gene.2014.11.001.

    Article  CAS  PubMed  Google Scholar 

  203. Xie, F., Wang, Q., Sun, R., & Zhang, B. (2015). Deep sequencing reveals important roles of microRNAs in response to drought and salinity stress in cotton. Journal of Experimental Botany, 66(3), 789–804. https://doi.org/10.1093/jxb/eru437.

    Article  CAS  PubMed  Google Scholar 

  204. Sun, G., Jr, C. N. S., Xiao, P., & Zhang, B. (2012). MicroRNA expression analysis in the cellulosic biofuel crop switchgrass (Panicum virgatum) under abiotic stress. PLoS One, 7(3), e32017. doi:https://doi.org/10.1371/journal.pone.0032017.

  205. Paul, S., Kundu, A., & Pal, A. (2011). Identification and validation of conserved microRNAs along with their differential expression in roots of Vigna unguiculata grown under salt stress. Plant Cell, Tissue and Organ Culture (PCTOC), 105(2), 233–242. https://doi.org/10.1007/s11240-010-9857-7.

    Article  CAS  Google Scholar 

  206. Frazier, T. P., Sun, G., Burklew, C. E., & Zhang, B. (2011). Salt and drought stresses induce the aberrant expression of microRNA genes in tobacco. Molecular Biotechnology, 49(2), 159–165. https://doi.org/10.1007/s12033-011-9387-5.

    Article  CAS  PubMed  Google Scholar 

  207. Khan, Y., Yadav, A., Bonthala, V. S., Muthamilarasan, M., Yadav, C. B., & Prasad, M. (2014). Comprehensive genome-wide identification and expression profiling of foxtail millet [Setaria italic (L.)] miRNAs in response to abiotic stress and development of miRNA database. Plant Cell, Tissue and Organ Culture (PCTOC), 118(2), 279–292. https://doi.org/10.1007/s11240-014-0480-x.

    Article  CAS  Google Scholar 

  208. Bottino, M. C., Rosario, S., Grativol, C., Thiebaut, F., Rojas, C. A., Farrineli, L., et al. (2013). High-throughput sequencing of small RNA transcriptome reveals salt stress regulated microRNAs in sugarcane. PLoS One, 8(3), e59423.

    Article  Google Scholar 

  209. Lelandais-Brière, C., Naya, L., Sallet, E., Calenge, F., Frugier, F., Hartmann, C., et al. (2009). Genome-wide Medicago truncatula small RNA analysis revealed novel microRNAs and isoforms differentially regulated in roots and nodules. The Plant Cell, 21(9), 2780–2796. https://doi.org/10.1105/tpc.109.068130.

    Article  PubMed  PubMed Central  Google Scholar 

  210. Zhang, J.-F., Yuan, L.-J., Shao, Y., Du, W. E. I., YAN, D.-W., & LU, Y.-T. (2008). The disturbance of small RNA pathways enhanced abscisic acid response and multiple stress responses in Arabidopsis. Plant, Cell & Environment, 31(4), 562–574 OK.

    Article  CAS  Google Scholar 

  211. Jia, X., Wang, W.-X., Ren, L., Chen, Q.-J., Mendu, V., Willcut, B., et al. (2009). Differential and dynamic regulation of miR398 in response to ABA and salt stress in Populus tremula and Arabidopsis thaliana, Plant Molecular Biology., 71(1–2), 51–59 OK.

  212. Jones-Rhoades, M. W., & Bartel, D. P. (2004). Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Molecular Cell, 14(6), 787–799.

    Article  CAS  PubMed  Google Scholar 

  213. Fang, Q., Xu, Z., & Song, R. (2006). Cloning, characterization and genetic engineering of FLC homolog in Thellungiella halophila. Biochemical and Biophysical Research Communications, 347(3), 707–714.

    Article  CAS  PubMed  Google Scholar 

  214. Cheng, Y., & Long, M. (2007). A cytosolic NADP-malic enzyme gene from rice (Oryza sativa L.) confers salt tolerance in transgenic Arabidopsis. Biotechnology Letters, 29(7), 1129–1134.

    Article  CAS  PubMed  Google Scholar 

  215. Yan, S., Tang, Z., Su, W., & Sun, W. (2005). Proteomic analysis of salt stress-responsive proteins in rice root. Proteomics, 5(1), 235–244.

    Article  CAS  PubMed  Google Scholar 

  216. Attia, H., Karray, N., Msilini, N., & Lachaâl, M. (2011). Effect of salt stress on gene expression of superoxide dismutases and copper chaperone in Arabidopsis thaliana. Biologia Plantarum, 55(1), 159–163.

    Article  CAS  Google Scholar 

  217. Wei, J.-Z., Tirajoh, A., Effendy, J., & Plant, A. L. (2000). Characterization of salt-induced changes in gene expression in tomato (Lycopersicon esculentum) roots and the role played by abscisic acid. Plant Science, 159(1), 135–148.

    Article  CAS  PubMed  Google Scholar 

  218. Covarrubias, A. A., & Reyes, J. L. (2010). Post-transcriptional gene regulation of salinity and drought responses by plant microRNAs. Plant, Cell & Environment, 33(4), 481–489.

    Article  CAS  Google Scholar 

  219. Pecinka, A., Dinh, H. Q., Baubec, T., Rosa, M., Lettner, N., & Mittelsten Scheid, O. (2010). Epigenetic regulation of repetitive elements is attenuated by prolonged heat stress in Arabidopsis. The Plant Cell, 22(9), 3118–3129. https://doi.org/10.1105/tpc.110.078493.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  220. González, R. M., Ricardi, M. M., & Iusem, N. D. (2013). Epigenetic marks in an adaptive water stress-responsive gene in tomato roots under normal and drought conditions. Epigenetics, 8(8), 864–872.

    Article  PubMed  PubMed Central  Google Scholar 

  221. Shafiq, S., & Khan, A. R. (2015). Plant epigenetics and crop improvement. In D. Barh, M. S. Khan, & E. Davies (Eds.), PlantOmics: the omics of plant science (pp. 157–179). Springer India. doi:https://doi.org/10.1007/978-81-322-2172-2_6.

  222. Choi, C.-S., & Sano, H. (2007). Abiotic-stress induces demethylation and transcriptional activation of a gene encoding a glycerophosphodiesterase-like protein in tobacco plants. Molecular Genetics and Genomics: MGG, 277(5), 589–600. https://doi.org/10.1007/s00438-007-0209-1.

    Article  CAS  PubMed  Google Scholar 

  223. Baek, D., Jiang, J., Chung, J.-S., Wang, B., Chen, J., Xin, Z., & Shi, H. (2010). Regulated AtHKT1 gene expression by a distal enhancer element and DNA methylation in the promoter plays an important role in salt tolerance. Plant and Cell Physiology, 52(1), 149–161.

    Article  CAS  PubMed  Google Scholar 

  224. Xu, R., Wang, Y., Zheng, H., Lu, W., Wu, C., Huang, J., et al. (2015). Salt-induced transcription factor MYB74 is regulated by the RNA-directed DNA methylation pathway in Arabidopsis. Journal of Experimental Botany, 66(19), 5997–6008. https://doi.org/10.1093/jxb/erv312.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  225. Kumar, S., Beena, A. S., Awana, M., & Singh, A. (2017). Salt-induced tissue-specific cytosine methylation downregulates expression of HKT genes in contrasting wheat (Triticum aestivum L.) genotypes. DNA and Cell Biology, 36(4), 283–294.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  226. Song, Y., Ji, D., Li, S., Wang, P., Li, Q., & Xiang, F. (2012). The dynamic changes of DNA methylation and histone modifications of salt responsive transcription factor genes in soybean. PLoS One, 7(7), e41274. doi:https://doi.org/10.1371/journal.pone.0041274.

  227. Lira-Medeiros, C. F., Parisod, C., Fernandes, R. A., Mata, C. S., Cardoso, M. A., & Ferreira, P. C. G. (2010). Epigenetic variation in mangrove plants occurring in contrasting natural environment. PLoS One, 5(4), e10326. https://doi.org/10.1371/journal.pone.0010326.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  228. Karan, R., DeLeon, T., Biradar, H., & Subudhi, P. K. (2012). Salt stress induced variation in DNA methylation pattern and its influence on gene expression in contrasting rice genotypes. PLoS One, 7(6), e40203. https://doi.org/10.1371/journal.pone.0040203.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  229. Lu, X. K., Shu, N., Wang, J. J., Chen, X. G., Wang, D. L., Wang, S., … Ye, W. W. (2017). Genome-wide analysis of salinity-stress induced DNA methylation alterations in cotton (Gossypium hirsutum L.) using the Me-DIP sequencing technology. Genetics and molecular research: GMR, 16(2).

  230. Al-Lawati, A., Al-Bahry, S., Victor, R., Al-Lawati, A. H., & Yaish, M. W. (2016). Salt stress alters DNA methylation levels in alfalfa (Medicago spp). Genetics and Molecular Research, 15(1).

  231. Pandey, G., Yadav, C. B., Sahu, P. P., Muthamilarasan, M., & Prasad, M. (2017). Salinity induced differential methylation patterns in contrasting cultivars of foxtail millet (Setaria italica L.) Plant Cell Reports, 36(5), 759–772.

    Article  CAS  PubMed  Google Scholar 

  232. Yang, F., Nie, H., & Xu, Y. H. (2013). Effect of salt stress on DNA methylation in Isatis indigotica. Journal of Chinese Medicinal Materials, 36(4), 515–518.

    CAS  PubMed  Google Scholar 

  233. Gao, X., Cao, D., Liu, J., Wang, X., Geng, S., Liu, B., & Shi, D. (2013). Tissue-specific and cation/anion-specific DNA methylation variations occurred in C. virgata in response to salinity stress. PloS One, 8(11), e78426.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  234. Marconi, G., Pace, R., Traini, A., Raggi, L., Lutts, S., Chiusano, M., … Albertini, E. (2013). Use of MSAP markers to analyse the effects of salt stress on DNA methylation in rapeseed (Brassica napus var. oleifera). PloS one, 8(9), e75597.

  235. Paul, A., Dasgupta, P., Roy, D., & Chaudhuri, S. (2017). Comparative analysis of histone modifications and DNA methylation at OsBZ8 locus under salinity stress in IR64 and Nonabokra rice varieties. Plant Molecular Biology, 95(1–2), 63–88.

    Article  CAS  PubMed  Google Scholar 

  236. Li, H., Yan, S., Zhao, L., Tan, J., Zhang, Q., Gao, F., et al. (2014). Histone acetylation associated up-regulation of the cell wall related genes is involved in salt stress induced maize root swelling. BMC Plant Biology, 14(1), 105. https://doi.org/10.1186/1471-2229-14-105.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  237. Sokol, A., Kwiatkowska, A., Jerzmanowski, A., & Prymakowska-Bosak, M. (2007). Up-regulation of stress-inducible genes in tobacco and Arabidopsis cells in response to abiotic stresses and ABA treatment correlates with dynamic changes in histone H3 and H4 modifications. Planta, 227(1), 245–254. https://doi.org/10.1007/s00425-007-0612-1.

    Article  CAS  PubMed  Google Scholar 

  238. Yolcu, S., Ozdemir, F., Güler, A., & Bor, M. (2016). Histone acetylation influences the transcriptional activation of POX in Beta vulgaris L. and Beta maritima L. under salt stress. Plant Physiology and Biochemistry: PPB, 100, 37–46. https://doi.org/10.1016/j.plaphy.2015.12.019.

    Article  CAS  PubMed  Google Scholar 

  239. Sani, E., Herzyk, P., Perrella, G., Colot, V., & Amtmann, A. (2013). Hyperosmotic priming of Arabidopsis seedlings establishes a long-term somatic memory accompanied by specific changes of the epigenome. Genome Biology, 14(6), 1–24. https://doi.org/10.1186/gb-2013-14-6-r59.

    Article  CAS  Google Scholar 

  240. Horie, T., Hauser, F., & Schroeder, J. I. (2009). HKT transporter-mediated salinity resistance mechanisms in Arabidopsis and monocot crop plants. Trends in Plant Science, 14(12), 660–668. https://doi.org/10.1016/j.tplants.2009.08.009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  241. Stroud, H., Do, T., Du, J., Zhong, X., Feng, S., Johnson, L., et al. (2014). Non-CG methylation patterns shape the epigenetic landscape in Arabidopsis. Nature Structural and Molecular Biology, 21(1), 64.

    Article  CAS  PubMed  Google Scholar 

  242. Feng, W., Dong, Z., He, B., & Wang, K. (2012). Analysis method of epigenetic DNA methylation to dynamically investigate the functional activity of transcription factors in gene expression. BMC Genomics, 13(1), 532.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  243. Hauser, M.-T., Aufsatz, W., Jonak, C., & Luschnig, C. (2011). Transgenerational epigenetic inheritance in plants. Biochimica et Biophysica Acta (BBA)—Gene Regulatory Mechanisms, 1809(8), 459–468. https://doi.org/10.1016/j.bbagrm.2011.03.007.

    Article  CAS  Google Scholar 

  244. Khan, A. R., Enjalbert, J., Marsollier, A.-C., Rousselet, A., Goldringer, I., & Vitte, C. (2013). Vernalization treatment induces site-specific DNA hypermethylation at the VERNALIZATION-A1 (VRN-A1) locus in hexaploid winter wheat. BMC Plant Biology, 13, 209. https://doi.org/10.1186/1471-2229-13-209.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  245. Mirouze, M., & Paszkowski, J. (2011). Epigenetic contribution to stress adaptation in plants. Current Opinion in Plant Biology, 14(3), 267–274. https://doi.org/10.1016/j.pbi.2011.03.004.

    Article  CAS  PubMed  Google Scholar 

  246. Feng, Q., Yang, C., Lin, X., Wang, J., Ou, X., Zhang, C., et al. (2012). Salt and alkaline stress induced transgenerational alteration in DNA methylation of rice ('Oryza sativa’). Australian Journal of Crop Science, 6(5), 877–883.

    CAS  Google Scholar 

  247. Boyko, A., Blevins, T., Yao, Y., Golubov, A., Bilichak, A., Ilnytskyy, Y., et al. (2010). Transgenerational adaptation of Arabidopsis to stress requires DNA methylation and the function of dicer-like proteins. PLoS One, 5(3), e9514. https://doi.org/10.1371/journal.pone.0009514.

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors thank Dr. Julie Dawson from University of Wisconsin-Madison for helping improve the English of the manuscript and COMSATS Institute of Information Technology, Abbottabad for providing all the facilities needed to complete this manuscript.

Author information

Authors and Affiliations

  1. Biotechnology Program, Department of Environmental Sciences, COMSATS Institute of Information Technology, Abbottabad, Pakistan

    Fawad Kaleem, Shahid Masood Shah & Abdul Rehman Khan

  2. Institute of Molecular Biology and Biotechnology, Bahauddin Zakariya University, Multan, Pakistan

    Ghulam Shabir, Kashif Aslam, Sumaira Rasul & Hamid Manzoor

Authors
  1. Fawad Kaleem
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ghulam Shabir
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kashif Aslam
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sumaira Rasul
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hamid Manzoor
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Shahid Masood Shah
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Abdul Rehman Khan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Abdul Rehman Khan.

Ethics declarations

Conflict of Interest

The authors declare that there is no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kaleem, F., Shabir, G., Aslam, K. et al. An Overview of the Genetics of Plant Response to Salt Stress: Present Status and the Way Forward. Appl Biochem Biotechnol 186, 306–334 (2018). https://doi.org/10.1007/s12010-018-2738-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12010-018-2738-y

Keywords

Search

Navigation